Cited by 129Neuroscience and Neuropharmacology ResearchVisual perception and processing mechanismsNeural dynamics and brain function

Modeling the Dynamic Interaction of Hebbian and Homeostatic Plasticity

Open access
Toyoizumi, Taro, Kaneko, Megumi, Stryker, Michael P., Miller, Kenneth D.·2014·Neuron

Abstract

Hebbian and homeostatic plasticity together refine neural circuitry, but their interactions are unclear. In most existing models, each form of plasticity directly modifies synaptic strength. Equilibrium is reached when the two are inducing equal and opposite changes. We show that such models cannot reproduce ocular dominance plasticity (ODP) because negative feedback from the slow homeostatic plasticity observed in ODP cannot stabilize the positive feedback of fast Hebbian plasticity. We propose a model in which synaptic strength is the product of a synapse-specific Hebbian factor and a postsynaptic-cell-specific homeostatic factor, with each factor separately arriving at a stable inactive state. This model captures ODP dynamics and has plausible biophysical substrates. We confirm model predictions experimentally that plasticity is inactive at stable states and that synaptic strength overshoots during recovery from visual deprivation. These results highlight the importance of multiple regulatory pathways for interactions of plasticity mechanisms operating over separate timescales.

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Crossref · 10.1016/j.neuron.2014.09.036

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  • If the contribution of CaMKII to synaptic transmission were a net gain that simply adds onto the preexisting excitatory drive of the cell, the system would be unstable and quickly saturate.

    “If this were the case, it has been argued that the system would be unstable and quickly saturate (366–371).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [370]

    The Introduction says that Hebbian plasticity is a positive-feedback process whose synaptic weights are typically unstable until they reach saturation. The Results discuss CaMKII as a possible mechanism of Hebbian LTP, but do not establish that CaMKII adds a net gain to preexisting excitatory drive or that this specific arrangement would quickly saturate. (LLM, conf=0.83)

    Experimental — accuracy not yet measured
  • The existence of LTD avoids the problem of saturation, which could be essential for a mnemonic device.

    “The existence of LTD avoids the problem of saturation, which could be essential for a mnemonic device (366–371).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [370]

    The Results section on single-synapse models describes LTD and says that both LTP and LTD should saturate, but does not say that the existence of LTD prevents synaptic saturation. The Discussion’s “Functional significance” section links maintained dynamic range to learning and memory, attributing it to the interaction of Hebbian and homeostatic plasticity rather than to LTD alone. I searched for the proposed LTD–saturation–memory link; no passage in our copy establishes it. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

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Research works printed but not linked: 44

  1. Antonini A Stryker MP Rapid remodeling of axonal arbors in the visual cortex Science 1993 260 1819 1821 8511592
  2. Atwood HL Karunanithi S Diversification of synaptic strength: presynaptic elements Nat Rev Neurosci 2002 3 497 516 12094207
  3. Bavelier D Levi DM Li RW Dan Y Hensch TK Removing brakes on adult brain plasticity: from molecular to behavioral interventions J Neurosci 2010 30 14964 71 21068299 PMC2992973
  4. Cho KKA Khibnik L Philpot BD Bear MF The ratio of nr2a/b nmda receptor subunits determines the qualities of ocular dominance plasticity in visual cortex Proc Natl Acad Sci U S A 2009 106 5377 5382 19276107 PMC2654025
  5. Cooper L Intrator N Blais B Shouval HZ Theory of cortical plasticity 2004 World Scientific Singapore
  6. Figurov A Pozzo-Miller LD Olafsson P Wang T Lu B Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus Nature 1996 381 706 709 8649517
  7. Frenkel MY Bear MF How monocular deprivation shifts ocular dominance in visual cortex of young mice Neuron 2004 44 917 923 15603735
  8. Gandhi SP Yanagawa Y Stryker MP Delayed plasticity of inhibitory neurons in developing visual cortex Proc Natl Acad Sci U S A 2008 105 16797 16802 18940923 PMC2575499
  9. Heynen A Yoon B Liu C Chung H Huganir R Bear M Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation Nat. Neurosci 2003 6 854 862 12886226
  10. Hofer S Mrsic-Flogel T Bonhoeffer T Hübener M Lifelong learning: ocular dominance plasticity in mouse visual cortex Curr. Opin. Neurobiol 2006 16 451 459 16837188
  11. Huganir RL Nicoll RA Ampars and synaptic plasticity: the last 25 years Neuron 2013 80 704 17 24183021 PMC4195488
  12. Kaneko M Cheetham CE Lee Y-SS Silva AJ Stryker MP Fox K Constitutively active h-ras accelerates multiple forms of plasticity in developing visual cortex Proc Natl Acad Sci U S A 2010 107 19026 31 20937865 PMC2973899
  13. Kaneko M Hanover J England P Stryker M TrkB kinase is required for recovery, but not loss, of cortical responses following monocular deprivation Nat. Neurosci 2008a 11 497 504 18311133 PMC2413329
  14. Kaneko M Stellwagen D Malenka R Stryker M Tumor necrosis factor-alpha mediates one component of competitive, experience-dependent plasticity in developing visual cortex Neuron 2008b 58 673 680 18549780 PMC2884387
  15. Kessels HW Malinow R Synaptic ampa receptor plasticity and behavior Neuron 2009 61 340 350 19217372 PMC3917551
  16. Kopec CD Real E Kessels HW Malinow R GluR1 links structural and functional plasticity at excitatory synapses J. Neurosci 2007 27 13706 13718 18077682 PMC6673607
  17. Kovalchuk Y Hanse E Kafitz KW Konnerth A Postsynaptic induction of bdnf-mediated long-term potentiation Science 2002 295 1729 1734 11872844
  18. Lai K-OO Wong ASL Cheung M-CC Xu P Liang Z Lok K-CC Xie H Palko ME Yung W-HH Tessarollo L Cheung ZH Ip NY Trkb phosphorylation by cdk5 is required for activity-dependent structural plasticity and spatial memory Nat Neurosci 2012 15 1506 15 23064382 PMC7511999
  19. Lee H-KK Takamiya K Han J-SS Man H Kim C-HH Rumbaugh G Yu S Ding L He C Petralia RS Wenthold RJ Gallagher M Huganir RL Phosphorylation of the ampa receptor glur1 subunit is required for synaptic plasticity and retention of spatial memory Cell 2003 112 631 43 12628184
  20. Leonoudakis D Zhao P Beattie EC Rapid tumor necrosis factor alpha-induced exocytosis of glutamate receptor 2-lacking AMPA receptors to extrasynaptic plasma membrane potentiates excitotoxicity J. Neurosci 2008 28 2119 30 18305246 PMC6671833
  21. Maffei A Nataraj K Nelson SB Turrigiano GG Potentiation of cortical inhibition by visual deprivation Nature 2006 443 81 84 16929304
  22. Miller KD Keller JB Stryker MP Ocular dominance column development: Analysis and simulation Science 1989 245 605 615 2762813
  23. Mrsic-Flogel TD Hofer SB Ohki K Reid RC Bonhoeffer T Hübener M Homeostatic regulation of eye-specific responses in visual cortex during ocular dominance plasticity Neuron 2007 54 961 972 17582335
  24. O’Connor DH Wittenberg GM Wang SS-H Graded bidirectional synaptic plasticity is composed of switch-like unitary events Proc Natl Acad Sci U S A 2005 102 9679 9684 15983385 PMC1172253
  25. Oja E A simplified neuron model as a principal component analyzer J. Mathematical Biology 1982 15 267 273 7153672
  26. Petersen CC Malenka RC Nicoll RA Hopfield JJ All-or-none potentiation at ca3-ca1 synapses Proc Natl Acad Sci U S A 1998 95 4732 7 9539807 PMC22559
  27. Pool RR Mato G Hebbian plasticity and homeostasis in a model of hyper-column of the visual cortex Neural Comput 2010 22 1837 1859 20235825
  28. Sato M Stryker MP Distinctive features of adult ocular dominance plasticity J Neurosci 2008 28 10278 10286 18842887 PMC2851628
  29. Sermasi E Margotti E Cattaneo A Domenici L Trk b signalling controls ltp but not ltd expression in the developing rat visual cortex Eur J Neurosci 2000 12 1411 1419 10762369
  30. Shepherd JD Huganir RL The cell biology of synaptic plasticity: Ampa receptor trafficking Annu Rev Cell Dev Biol 2007 23 613 643 17506699
  31. Steinmetz CC Turrigiano GG Tumor necrosis factor-α signaling maintains the ability of cortical synapses to express synaptic scaling The Journal of neuroscience 2010 30 14685 90 21048125 PMC3063078
  32. Stellwagen D Malenka R Synaptic scaling mediated by glial TNF-alpha Nature 2006 440 1054 1059 16547515
  33. Sun Q Turrigiano GG PSD-95 and PSD-93 play critical but distinct roles in synaptic scaling up and down The Journal of neuroscience 2011 31 6800 8 21543610 PMC3113607
  34. Taha S Hanover JL Silva AJ Stryker MP Autophosphorylation of alphacamkii is required for ocular dominance plasticity Neuron 2002 36 483 91 12408850
  35. Taha S Stryker MP Rapid ocular dominance plasticity requires cortical but not geniculate protein synthesis Neuron 2002 34 425 36 11988173
  36. Toyoizumi T Miller KD Equalization of ocular dominance columns induced by an activity-dependent learning rule and the maturation of inhibition J Neurosci 2009 29 6514 6525 19458222 PMC2923481
  37. Toyoizumi T Miyamoto H Yazaki-Sugiyama Y Atapour N Hencsh TK Miller KD A theory of the transition to critical period plasticity: Inhibition suppresses spontaneous relative to sensory-driven activity Neuron 2013 80 51 63 24094102 PMC3800182
  38. Trachtenberg J Stryker M Rapid anatomical plasticity of horizontal connections in the developing visual cortex J. Neurosci 2001 21 3476 82 11331376 PMC2452996
  39. Turrigiano G Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement Annu. Rev. Neurosci 2011 34 89 103 21438687
  40. Turrigiano GG The self-tuning neuron: synaptic scaling of excitatory synapses Cell 2008 135 422 435 18984155 PMC2834419
  41. Turrigiano GG Leslie KR Desai NS Rutherford LC Nelson SB Activity-dependent scaling of quantal amplitude in neocortical neurons Nature 1998 391 892 896 9495341
  42. von der Malsburg C Self-organization of orientation selective cells in the striate cortex Kybernetik 1973 14 85 100 4786750
  43. Yoon B-J Smith GB Heynen AJ Neve RL Bear MF Essential role for a long-term depression mechanism in ocular dominance plasticity Proc Natl Acad Sci U S A 2009 106 9860 9865 19470483 PMC2685742
  44. Zenke F Hennequin G Gerstner W Synaptic plasticity in neural networks needs homeostasis with a fast rate detector PLoS Comput Biol 2013 9 e1003330 24244138 PMC3828150

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Authors
Toyoizumi, T., Kaneko, M., Stryker, M. P., & Miller, K. D.
Affiliations
  • Tokyo Institute of Technology (JP)
  • University of California, San Francisco (US)
  • Columbia University (US)
Corresponding author
Toyoizumi, Taro
Venue
Neuron
Publisher
Elsevier BV
Published
2014-10
Volume
84
Issue
2
Pages
497-510
ISSN
0896-6273 (ISSN-L)
OpenAlex
W2102744370
Cited by
129
References
11
Citations by year
2026: 3 · 2025: 12 · 2024: 18 · 2023: 15 · 2022: 10 · 2021: 9 · 2020: 10 · 2019: 6 · 2018: 11 · 2017: 18 · 2016: 9 · 2015: 8
FWCI
5.34
Type
journal article
Language
en
Open access
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • National Institute of Mental Health (T32MH089920)
  • National Eye Institute (R01EY011001, R01-EY02874, EY11001, R01EY002874)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
Hebbian plasticity, homeostatic plasticity, ocular dominance plasticity, synaptic efficacy, visual deprivation, negative feedback, positive feedback, synaptic scaling, neural circuit refinement
MeSH terms
Animals, Feedback, Homeostasis, Male, Mice, Inbred C57BL, Models, Neurological, Neuronal Plasticity, Neurons, Synapses, Time Factors, Dominance, Ocular

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